Heal Katherine R, Durham Bryndan P, Boysen Angela K, Carlson Laura T, Qin Wei, Ribalet François, White Angelicque E, Bundy Randelle M, Armbrust E Virginia, Ingalls Anitra E
School of Oceanography, University of Washington, Seattle, Washington, USA.
Department of Biology, Genetics Institute, University of Florida, Gainesville, Florida, USA.
mSystems. 2021 May 4;6(3):e01334-20. doi: 10.1128/mSystems.01334-20.
Phytoplankton transform inorganic carbon into thousands of biomolecules that represent an important pool of fixed carbon, nitrogen, and sulfur in the surface ocean. Metabolite production differs between phytoplankton, and the flux of these molecules through the microbial food web depends on compound-specific bioavailability to members of a wider microbial community. Yet relatively little is known about the diversity or concentration of metabolites within marine plankton. Here, we compare 313 polar metabolites in 21 cultured phytoplankton species and in natural planktonic communities across environmental gradients to show that bulk community metabolomes reflect the chemical composition of the phytoplankton community. We also show that groups of compounds have similar patterns across space and taxonomy, suggesting that the concentrations of these compounds in the environment are controlled by similar sources and sinks. We quantify several compounds in the surface ocean that represent substantial understudied pools of labile carbon. For example, the N-containing metabolite homarine was up to 3% of particulate carbon and is produced in high concentrations by cultured , and S-containing gonyol accumulated up to 2.5 nM in surface particles and likely originates from dinoflagellates or haptophytes. Our results show that phytoplankton composition directly shapes the carbon composition of the surface ocean. Our findings suggest that in order to access these pools of bioavailable carbon, the wider microbial community must be adapted to phytoplankton community composition. Microscopic phytoplankton transform 100 million tons of inorganic carbon into thousands of different organic compounds each day. The structure of each chemical is critical to its biological and ecosystem function, yet the diversity of biomolecules produced by marine microbial communities remained mainly unexplored, especially small polar molecules which are often considered the currency of the microbial loop. Here, we explore the abundance and diversity of small biomolecules in planktonic communities across ecological gradients in the North Pacific and within 21 cultured phytoplankton species. Our work demonstrates that phytoplankton diversity is an important determinant of the chemical composition of the highly bioavailable pool of organic carbon in the ocean, and we highlight understudied yet abundant compounds in both the environment and cultured organisms. These findings add to understanding of how the chemical makeup of phytoplankton shapes marine microbial communities where the ability to sense and use biomolecules depends on the chemical structure.
浮游植物将无机碳转化为数千种生物分子,这些生物分子代表了海洋表层中一个重要的固定碳、氮和硫库。不同浮游植物的代谢产物产量有所不同,这些分子通过微生物食物网的通量取决于更广泛微生物群落成员对特定化合物的生物可利用性。然而,对于海洋浮游生物中代谢产物的多样性或浓度,我们了解得相对较少。在这里,我们比较了21种培养的浮游植物物种和跨环境梯度的自然浮游生物群落中的313种极性代谢产物,以表明整体群落代谢组反映了浮游植物群落的化学组成。我们还表明,化合物组在空间和分类学上具有相似的模式,这表明这些化合物在环境中的浓度受相似的源和汇控制。我们对海洋表层中的几种化合物进行了量化,这些化合物代表了大量尚未得到充分研究的不稳定碳库。例如,含氮代谢产物高牛磺酸占颗粒碳的比例高达3%,并且在培养物中大量产生,而含硫的冈田酸在表层颗粒中积累高达2.5 nM,可能源自甲藻或定鞭藻。我们的结果表明,浮游植物组成直接塑造了海洋表层的碳组成。我们的研究结果表明,为了获取这些生物可利用碳库,更广泛的微生物群落必须适应浮游植物群落组成。微小的浮游植物每天将1亿吨无机碳转化为数千种不同的有机化合物。每种化学物质的结构对其生物学和生态系统功能至关重要,然而,海洋微生物群落产生的生物分子的多样性仍主要未被探索,尤其是那些常被视为微生物环流通货币的小极性分子。在这里,我们探讨了北太平洋生态梯度上的浮游生物群落以及21种培养的浮游植物物种中生物小分子的丰度和多样性。我们的工作表明,浮游植物多样性是海洋中高度生物可利用有机碳库化学组成的重要决定因素,并且我们强调了环境和培养生物中尚未得到充分研究但含量丰富的化合物。这些发现有助于理解浮游植物的化学组成如何塑造海洋微生物群落,在这个群落中,感知和利用生物分子的能力取决于化学结构。